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Development of Theta Rhythmicity in Entorhinal Stellate Cells of the Juvenile Rat

Department of Biomedical Engineering, Center for Memory and Brain, Center for BioDynamics, Boston University, Boston, Massachusetts

Submitted 31 March 2008; accepted in final form 29 September 2008

Mature stellate cells of the rat medial entorhinal cortex (EC), layer II, exhibit subthreshold membrane potential oscillations (MPOs) at theta frequencies (4–12 Hz) in vitro. We find that MPOs appear between postnatal days 14 (P14) and 18 (P18) but show little further change by day 28+ (P28–P32). To identify the factors responsible, we examined the electrical responses of developing stellate cells, paying attention to two currents thought necessary for mature oscillation: the h current I_h, which provides the slow rectification required for resonance; and a persistent sodium current I_NaP, which provides amplification of resonance. Responses to injected current revealed that P14 cells were often nonresonant with a relatively high resistance. Densities of I_h and I_NaP both rose by about 50% from P14 to P18. However, I_h levels fell to intermediate values by P28+. Given the nonrobust trend in I_h expression and a previously demonstrated potency of even low levels of I_h to sustain oscillation, we propose that resonance and MPOs are limited at P14 more by low levels of I_NaP than of I_h. The relative importance of I_NaP for the development of MPOs is supported by simulations of a conductance-based model, which also suggest that general shunt conductance may influence the precise age when MPOs appear. In addition to our physiological study, we analyzed spine densities at P14, P18, and P28+ and found a vigorous synaptogenesis across the whole period. Our data predict that functions that rely on theta rhythmicity in the hippocampal network are limited until at least P18.